An undigested gliadin peptide activates innate immunity and proliferative signaling in enterocytes: The role in celiac disease

American Journal of Clinical Nutrition

Volumn 98, Issue 4, 2013, Pages 1123-1135

  Nanayakkara, Merlin ^a   Lania, Giuliana ^a   Maglio, Mariantonia ^a   Discepolo, Valentina ^a,b   Sarno, Marco ^a   Gaito, Alessandra ^a   Troncone, Riccardo ^a   Auricchio, Salvatore ^a   Auricchio, Renata ^a   Barone, Maria Vittoria ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOCKING ANTIBODY; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GLIADIN; INTERLEUKIN 15; MESSENGER RNA; P 3143 PEPTIDE; STAT5 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELIAC DISEASE; CELL PROLIFERATION; CELL STRAIN CACO 2; COMPLEX FORMATION; CONTROLLED STUDY; DUODENUM BIOPSY; INNATE IMMUNITY; INTESTINE BIOPSY; INTESTINE CELL; INTESTINE EPITHELIUM CELL; LIGAND BINDING; MOLECULAR DYNAMICS; POLYMERASE CHAIN REACTION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANTIBODIES; CACO-2 CELLS; CELIAC DISEASE; CELL PROLIFERATION; CELLS, CULTURED; ENTEROCYTES; EPIDERMAL GROWTH FACTOR; GENE EXPRESSION REGULATION; GLIADIN; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-15; INTERLEUKIN-15 RECEPTOR ALPHA SUBUNIT; PEPTIDE FRAGMENTS; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84884857478     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.112.054544     Document Type: Article

References (40)

1. Osborne O, Olefsky GM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 2012;18: 366-74.
2. Li Y, Innocentin S,Withers DR, Roberts NA, Gallagher AR, Grigorieva EF, Wilhelm C, Veldhoen M. Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation. Cell 2011;147:629-40.
3. Diosdado B, Wapenaar MC, Franke L, Duran KJ, Goerres MJ, Hadithi M, Crusius JB, Meijer JW, Duggan DJ, Mulder CJ, et al. A microarray screen for novel candidate genes in coeliac disease pathogenesis. Gut 2004;53:944-51. (Pubitemid 38824150)
4. Juuti-Uusitalo K, Maki M, Kainulainen H, Isola J, Kaukinen K. Gluten affects epithelial differentiation-associated genes in small intestinal mucosa of coeliac patients. Clin Exp Immunol 2007;150:294-305. (Pubitemid 47609574)
5. Marsh MN, Loft DE, Garner VG. Time dose responses of coeliac mucosae to graded oral challenges with Frazer's Fraction III (FF3) of gliadin. Eur Gastroenterol Hepatol. 1992;4:667-74.
6. Marsh MN. Clinical and pathological spectrum of coeliac disease. Gut 1993;34:1740.
7. Marsh MN, Crowe PT. Morphology of the mucosal lesion in gluten sensitivity. Baillieres Clin Gastroenterol 1995;9:273-93.
8. Sollid LM. Molecular basis of celiac disease. Annu Rev Immunol 2000;18:53-81. (Pubitemid 30365374)
9. Maiuri L, Ciacci C, Ricciardelli I, Vacca L, Raia V, Auricchio S, Picard J, Osman M, Quaratino S, Londei M. Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease. Lancet 2003;362:30-7. (Pubitemid 36835817)
10. Hüe S, Mention JJ, Monteiro RC, Zhang S, Cellier C, Schmitz J, Verkarre V, Fodil N, Bahram S, Cerf-Bensussan N, et al. A direct role for NKG2D/MICA interaction in villous atrophy during celiac disease. Immunity 2004;21:367-77. (Pubitemid 39208338)
11. Barone MV, Gimigliano A, Castoria G, Paolella G, Maurano F, Maglio M, Mineo A, Miele E, Nanayakkara M, Troncone R, et al. Growth factor-like activity of gliadin, an alimentary protein: implications for coeliac disease. Gut 2007;56:480-8. (Pubitemid 46580502)
12. Barone MV, Nanayakkara M, Paolella G, Maglio M, Vitale V, Troiano R, Ribecco MT, Lania G, Zanzi D, Santagata S, et al. Gliadin peptide P31-43 localises to endocytic vesicles and interferes with their maturation. PLoS ONE 2010;5:e12246.
13. Barone MV, Zanzi D, Maglio M, Nanayakkara M, Santagata S, Lania G, Miele E, Ribecco MT, Maurano F, Auricchio R, et al. Gliadinmediated proliferation and innate immune activation in celiac disease are due to alterations in vesicular trafficking. PLoS ONE 2011;6: e17039.
14. Shan L, Molberg Ø, Parrot I, Hausch F, Filiz F, Gray GM, Sollid LM, Khosla C. Structural basis for gluten intolerance in celiac sprue. Science 2002;297:2275-9.
15. Comino I, Real A, Vivas S, Síglez MÁ , Caminero A, Nistal E, Casqueiro J, Rodríguez-Herrera A, Cebolla A, Sousa C. Monitoring of gluten-free diet compliance in celiac patients by assessment of gliadin 33-mer equivalent epitopes in feces. Am J Clin Nutr 2012;95:670-7.
16. Mamone G, Ferranti P, Rossi M, Roepstorff P, Fierro O, Malorni A, Addeo F. Identification of a peptide from alpha-gliadin resistant to digestive enzymes: implications for celiac disease. J Chromatogr B Analyt Technol Biomed Life Sci 2007;855:236-41. (Pubitemid 47212017)
17. Zimmer KP, Fischer I, Mothes T, Weissen-Plenz G, Schmitz M, Wieser H, Büning J, Lerch MM, Ciclitira PC, Weber P, et al. Endocytotic segregation of gliadin peptide 31-49 in enterocytes. Gut 2010;59: 300-10.
18. Maiuri L, Ciacci C, Vacca L, Ricciardelli I, Auricchio S, Quaratino S, Londei M. IL-15 drives the specific migration of CD94+ and TCRgammadelta+ intraepithelial lymphocytes in organ cultures of treated celiac patients. Am J Gastroenterol 2001;96:150-6. (Pubitemid 32104823)
19. Mention JJ, Ben Ahmed M, Bègue B, Barbe U, Verkarre V, Asnafi V, Colombel JF, Cugnenc PH, Ruemmele FM, McIntyre E, et al. Interleukin 15: a key to disrupted intraepithelial lymphocyte homeostasis and lymphomagenesis in celiac disease. Gastroenterology 2003;125: 730-45. (Pubitemid 37070691)
20. Maiuri L, Ciacci C, Auricchio S, Brown V, Quaratino S, Londei M. Interleukin 15 mediates epithelial changes in celiac disease. Gastroenterology 2000;119:996-1006.
21. Meresse B, Chen Z, Ciszewski C, Tretiakova M, Bhagat G, Krausz TN, Raulet DH, Lanier LL, Groh V, Spies T, et al. Coordinated induction by IL-15 of a TCR-independent NKG2D signaling pathway converts CTL into lymphokine-activated killer cells in celiac disease. Immunity 2004;21:357-66. (Pubitemid 39208337)
22. Di Sabatino A, Ciccocioppo R, Cupelli F, Cinque B, Millimaggi D, Clarkson MM, Paulli M, Cifone MG, Corazza GR. Epithelium derived interleukin 15 regulates intraepithelial lymphocyte Th1 cytokine production, cytotoxicity, and survival in coeliac disease. Gut 2006;55: 469-77.
23. Barone MV, Sepe L, Melillo RM, Mineo A, Santelli G, Monaco C, Castellone MD, Tramontano D, Fusco A, Santoro M. RET/PTC1 oncogene signaling in PC Cl 3 thyroid cells requires the small GTPbinding protein Rho. Oncogene 2001;20:6973-82. (Pubitemid 33052190)
24. Lombardi M, Castoria G, Migliaccio A, Barone MV, Di Stasio R, Ciociola A, Bottero D, Yamaguchi H, Appella E, Auricchio F. Hormone- dependent nuclear export of estradiol receptor and DNA synthesis in breast cancer cells. J Cell Biol 2008;182:327-40.
25. Colucci-D'Amato GL, D'Alessio A, Califano D, Cali G, Rizzo C, Nitsch L, Santelli G, de Franciscis V. Abrogation of nerve growth factor-induced terminal differentiation by ret oncogene involves perturbation of nuclear translocation of ERK. J Biol Chem 2000;275: 19306-14. (Pubitemid 30422904)
26. Barone MV, Caputo I, Ribecco MT, Maglio M, Marzari R, Sblattero D, Troncone R, Auricchio S, Esposito C. Humoral immune response to tissue transglutaminase is related to epithelial cell proliferation in celiac disease. Gastroenterology 2007;132:1245-53. (Pubitemid 46627567)
27. Quesnelle KM, Boehm AL, Grandis JR. STAT-mediated EGFR signaling in cancer. J Cell Biochem 2007;102:311-9. (Pubitemid 47519405)
28. Adunyah SE, Wheeler BJ, Cooper RS. Evidence for the involvement of LCK and MAP kinase (ERK-1) in the signal transduction mechanism of interleukin-15. Biochem Biophys Res Commun 1997;232:754-758. (Pubitemid 27214071)
29. Murphy MS. Growth factors and the gastrointestinal tract. Nutrition 1998;14:771-4. (Pubitemid 28460276)
30. Reinecker HC, MacDermott RP, Mirau S, Dignass A, Podolsky DK. Intestinal epithelial cells both express and respond to interleukin 15. Gastroenterology 1996;111:1706-13. (Pubitemid 26404238)
31. Juuti-Uusitalo K, Lindfors K, Mäki M, Patrikainen M, Isola J, Kaukinen K. Inhibition of epithelial growth factor receptor signaling does not preserve epithelial barrier function after in vitro gliadin insult. Scand J Gastroenterol 2009;44:820-5.
32. Qiu Y, Ravi L, Kung HJ. Requirement of ErbB2 for signaling by interleukin- 6 in prostate carcinoma cells. Nature 1998;393:83-5. (Pubitemid 28240259)
33. Colón E, Svechnikov KV, Carlsson-Skwirut C, Bang P, Soder O. Stimulation of steroidogenesis in immature rat Leydig cells evoked by interleukin-1alpha is potentiated by growth hormone and insulin-like growth factors. Endocrinology 2005;146:221-30. (Pubitemid 40051743)
34. DePaolo RW, Abadie V, Tang F, Fehlner-Peach H, Hall JA, Wang W, Marietta EV, Waldmann TA, Murray JA, Semrad C, et al. Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens. Nature 2011;471:220-4.
35. Lewkowicz P, Tchórzewski H, Dytnerska K, Banasik M, Lewkowicz N. Epidermal growth factor enhances TNF-alpha-induced priming of human neutrophils. Immunol Lett 2005;96:203-10. (Pubitemid 39600776)
36. Boughan PK, Argent RH, Body-Malapel M, Park JH, Ewings KE, Bowie AG, Ong SJ, Cook SJ, Sorensen OE, Manzo BA, et al. Nucleotide- binding oligomerization domain-1 and epidermal growth factor receptor: critical regulators of beta-defensins during Helicobacter pYlori infection. J Biol Chem 2006;281:11637-48. (Pubitemid 43855421)
37. Burgel PR, Nadel JA. Epidermal growth factor receptor-mediated innate immune responses and their roles in airway diseases. Eur Respir J 2008;32:1068-81.
38. Johnston A, Gudjonsson JE, Aphale A, Guzman AM, Stoll SW, Elder JT. EGFR and IL-1 signaling synergistically promote keratinocyte antimicrobial defenses in a differentiation-dependent manner. J Invest Dermatol 2011;131:329-37.
39. Burgess AW. Growth control mechanisms in normal and transformed intestinal cells. Philos Trans R Soc Lond B Biol Sci 1998;353:903-9. (Pubitemid 28314372)
40. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011;469:415-8.